Deep mitochondrial divergence can be explained by ghost introgression.
Extinct species can leave traces in the genomes of modern species. Human DNA, for example, contains genetic material from at least two extinct species, Neanderthals and Denisovans. And last year scientists found remnants of Cave Bear DNA (about 0.9 to 2.4 percent) in modern Brown Bears. These patterns are the result of ancient hybridization events between the species under investigation. Given the common occurrence of hybridization in birds, we can expect to find similar cases in our feathered friends. A recent study in the journal Molecular Biology and Evolution provides evidence for such a case.
The Tickell’s Leaf Warbler species complex contains three species: the nominal Tickell’s Leaf Warbler (Phylloscopus affinis), the Alpine Leaf-warbler (P. occisinensis) and the Sulphur-bellied Warbler (P. griseolus). The Alpine Leaf-warbler was only recently recognized as a distinct species, mainly based on divergence in the mitochondrial DNA. Analyses of this circular genome revealed that the Alpine Leaf-warbler diverged from the Tickell’s Leaf Warbler about four million years ago. However, the nuclear genome of these species is very similar, pointing to a speciation event only 600,000 years ago.
This phenomenon is called deep mitochondrial divergence (DMD) and can be caused by several evolutionary processes. Let’s have a look at the possibilities.
When females stay in the breeding areas and males disperse widely, mitochondrial DNA (which is only inherited through the female line) can diverge while the nuclear genome (which is inherited from both parents) remains undifferentiated. However, this scenario is unlikely because females are generally the dispersing sex in passerines. So, we can easily reject this explanation.
DMD can be due to an ancient differentiation event of mtDNA that did not involve nuclear DNA. This has been observed in some brood-parasitic birds and seems to be associated with host shifts of females. Because females show different behavior while males keep mating randomly, only female-linked traits (such as mtDNA and the W-chromosome) diverge. This results in mitochondrial divergence without nuclear differentiation. Because Leaf Warblers don’t show such female-specific behavior, the authors deem it unlikely that ancient divergence can explain DMD.
However, a recent study on the Savannah Sparrow (Passerculus sandwichensis) showed that divergent mitochondrial lineages can originate within a large panmictic population (see this blog post). They estimated that an effective population size of more than 350,000 is necessary for this to occur. The analyses of the Leaf Warblers show a peak in effective population size around 500,000, indicating that the mitochondrial divergence could have arisen within a large population.
The final possible explanation for DMD is ghost introgression: an extinct species of Leaf Warbler hybridized with the ancestor of present-day birds, resulting in the exchange of mtDNA. This idea is supported by some peculiar patterns in the nuclear genome. The researchers find several diverged regions in the nuclear genome and consider these remnants of the ancient hybridization events that resulted in the mtDNA transfer.
Although a scenario of ancient introgression is certainly possible, I am not sure if the researchers can reach this conclusion based on the current evidence. The possibility of DMD arising in a sufficiently large population (as explained above) makes me hesitant to declare the ghost introgression hypothesis as the winning explanation. More research is needed to discriminate between these explanations. One could, for example, test different introgression scenarios using Approximate Bayesian Computation (ABC) with deep learning, which has been done on human data. To be continued…
Barlow et al. (2018). Partial genomic survival of cave bears in living brown bears. Nature Ecology & Evolution, 2(10), 1563.
Benham & Cheviron (2019). Divergent mitochondrial lineages arose within a large, panmictic population of the Savannah sparrow (Passerculus sandwichensis). Molecular Ecology. 28(7), 1765-1783.
Martens et al. (2008). Intraspecific differentiation of Sino-Himalayan bush-dwelling Phylloscopus leaf warblers, with description of two new taxa. (P. fuscatus, P. fuligiventer, P. affinis, P. armandii, P. subaffinis). Vertebrate Zoology. 58(2):233-265.
Mondal et al. (2019). Approximate Bayesian computation with deep learning supports a third archaic introgression in Asia and Oceania. Nature communications, 10(1), 246.
Zhang, D. et al. (2019). “Ghost Introgression” As a Cause of Deep Mitochondrial Divergence in a Bird Species Complex. Molecular Biology and Evolution.
This paper has been added to the Phylloscopidae page.